Cargando…

Coordination of peptidoglycan synthesis and outer membrane constriction during Escherichia coli cell division

To maintain cellular structure and integrity during division, Gram-negative bacteria must carefully coordinate constriction of a tripartite cell envelope of inner membrane, peptidoglycan (PG), and outer membrane (OM). It has remained enigmatic how this is accomplished. Here, we show that envelope ma...

Descripción completa

Detalles Bibliográficos
Autores principales: Gray, Andrew N, Egan, Alexander JF, van't Veer, Inge L, Verheul, Jolanda, Colavin, Alexandre, Koumoutsi, Alexandra, Biboy, Jacob, Altelaar, A F Maarten, Damen, Mirjam J, Huang, Kerwyn Casey, Simorre, Jean-Pierre, Breukink, Eefjan, den Blaauwen, Tanneke, Typas, Athanasios, Gross, Carol A, Vollmer, Waldemar
Formato: Online Artículo Texto
Lenguaje:English
Publicado: eLife Sciences Publications, Ltd 2015
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4458516/
https://www.ncbi.nlm.nih.gov/pubmed/25951518
http://dx.doi.org/10.7554/eLife.07118
_version_ 1782375088256974848
author Gray, Andrew N
Egan, Alexander JF
van't Veer, Inge L
Verheul, Jolanda
Colavin, Alexandre
Koumoutsi, Alexandra
Biboy, Jacob
Altelaar, A F Maarten
Damen, Mirjam J
Huang, Kerwyn Casey
Simorre, Jean-Pierre
Breukink, Eefjan
den Blaauwen, Tanneke
Typas, Athanasios
Gross, Carol A
Vollmer, Waldemar
author_facet Gray, Andrew N
Egan, Alexander JF
van't Veer, Inge L
Verheul, Jolanda
Colavin, Alexandre
Koumoutsi, Alexandra
Biboy, Jacob
Altelaar, A F Maarten
Damen, Mirjam J
Huang, Kerwyn Casey
Simorre, Jean-Pierre
Breukink, Eefjan
den Blaauwen, Tanneke
Typas, Athanasios
Gross, Carol A
Vollmer, Waldemar
author_sort Gray, Andrew N
collection PubMed
description To maintain cellular structure and integrity during division, Gram-negative bacteria must carefully coordinate constriction of a tripartite cell envelope of inner membrane, peptidoglycan (PG), and outer membrane (OM). It has remained enigmatic how this is accomplished. Here, we show that envelope machines facilitating septal PG synthesis (PBP1B-LpoB complex) and OM constriction (Tol system) are physically and functionally coordinated via YbgF, renamed CpoB (Coordinator of PG synthesis and OM constriction, associated with PBP1B). CpoB localizes to the septum concurrent with PBP1B-LpoB and Tol at the onset of constriction, interacts with both complexes, and regulates PBP1B activity in response to Tol energy state. This coordination links PG synthesis with OM invagination and imparts a unique mode of bifunctional PG synthase regulation by selectively modulating PBP1B cross-linking activity. Coordination of the PBP1B and Tol machines by CpoB contributes to effective PBP1B function in vivo and maintenance of cell envelope integrity during division. DOI: http://dx.doi.org/10.7554/eLife.07118.001
format Online
Article
Text
id pubmed-4458516
institution National Center for Biotechnology Information
language English
publishDate 2015
publisher eLife Sciences Publications, Ltd
record_format MEDLINE/PubMed
spelling pubmed-44585162015-06-10 Coordination of peptidoglycan synthesis and outer membrane constriction during Escherichia coli cell division Gray, Andrew N Egan, Alexander JF van't Veer, Inge L Verheul, Jolanda Colavin, Alexandre Koumoutsi, Alexandra Biboy, Jacob Altelaar, A F Maarten Damen, Mirjam J Huang, Kerwyn Casey Simorre, Jean-Pierre Breukink, Eefjan den Blaauwen, Tanneke Typas, Athanasios Gross, Carol A Vollmer, Waldemar eLife Microbiology and Infectious Disease To maintain cellular structure and integrity during division, Gram-negative bacteria must carefully coordinate constriction of a tripartite cell envelope of inner membrane, peptidoglycan (PG), and outer membrane (OM). It has remained enigmatic how this is accomplished. Here, we show that envelope machines facilitating septal PG synthesis (PBP1B-LpoB complex) and OM constriction (Tol system) are physically and functionally coordinated via YbgF, renamed CpoB (Coordinator of PG synthesis and OM constriction, associated with PBP1B). CpoB localizes to the septum concurrent with PBP1B-LpoB and Tol at the onset of constriction, interacts with both complexes, and regulates PBP1B activity in response to Tol energy state. This coordination links PG synthesis with OM invagination and imparts a unique mode of bifunctional PG synthase regulation by selectively modulating PBP1B cross-linking activity. Coordination of the PBP1B and Tol machines by CpoB contributes to effective PBP1B function in vivo and maintenance of cell envelope integrity during division. DOI: http://dx.doi.org/10.7554/eLife.07118.001 eLife Sciences Publications, Ltd 2015-05-07 /pmc/articles/PMC4458516/ /pubmed/25951518 http://dx.doi.org/10.7554/eLife.07118 Text en © 2015, Gray et al http://creativecommons.org/licenses/by/4.0/ This article is distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use and redistribution provided that the original author and source are credited.
spellingShingle Microbiology and Infectious Disease
Gray, Andrew N
Egan, Alexander JF
van't Veer, Inge L
Verheul, Jolanda
Colavin, Alexandre
Koumoutsi, Alexandra
Biboy, Jacob
Altelaar, A F Maarten
Damen, Mirjam J
Huang, Kerwyn Casey
Simorre, Jean-Pierre
Breukink, Eefjan
den Blaauwen, Tanneke
Typas, Athanasios
Gross, Carol A
Vollmer, Waldemar
Coordination of peptidoglycan synthesis and outer membrane constriction during Escherichia coli cell division
title Coordination of peptidoglycan synthesis and outer membrane constriction during Escherichia coli cell division
title_full Coordination of peptidoglycan synthesis and outer membrane constriction during Escherichia coli cell division
title_fullStr Coordination of peptidoglycan synthesis and outer membrane constriction during Escherichia coli cell division
title_full_unstemmed Coordination of peptidoglycan synthesis and outer membrane constriction during Escherichia coli cell division
title_short Coordination of peptidoglycan synthesis and outer membrane constriction during Escherichia coli cell division
title_sort coordination of peptidoglycan synthesis and outer membrane constriction during escherichia coli cell division
topic Microbiology and Infectious Disease
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4458516/
https://www.ncbi.nlm.nih.gov/pubmed/25951518
http://dx.doi.org/10.7554/eLife.07118
work_keys_str_mv AT grayandrewn coordinationofpeptidoglycansynthesisandoutermembraneconstrictionduringescherichiacolicelldivision
AT eganalexanderjf coordinationofpeptidoglycansynthesisandoutermembraneconstrictionduringescherichiacolicelldivision
AT vantveeringel coordinationofpeptidoglycansynthesisandoutermembraneconstrictionduringescherichiacolicelldivision
AT verheuljolanda coordinationofpeptidoglycansynthesisandoutermembraneconstrictionduringescherichiacolicelldivision
AT colavinalexandre coordinationofpeptidoglycansynthesisandoutermembraneconstrictionduringescherichiacolicelldivision
AT koumoutsialexandra coordinationofpeptidoglycansynthesisandoutermembraneconstrictionduringescherichiacolicelldivision
AT biboyjacob coordinationofpeptidoglycansynthesisandoutermembraneconstrictionduringescherichiacolicelldivision
AT altelaarafmaarten coordinationofpeptidoglycansynthesisandoutermembraneconstrictionduringescherichiacolicelldivision
AT damenmirjamj coordinationofpeptidoglycansynthesisandoutermembraneconstrictionduringescherichiacolicelldivision
AT huangkerwyncasey coordinationofpeptidoglycansynthesisandoutermembraneconstrictionduringescherichiacolicelldivision
AT simorrejeanpierre coordinationofpeptidoglycansynthesisandoutermembraneconstrictionduringescherichiacolicelldivision
AT breukinkeefjan coordinationofpeptidoglycansynthesisandoutermembraneconstrictionduringescherichiacolicelldivision
AT denblaauwentanneke coordinationofpeptidoglycansynthesisandoutermembraneconstrictionduringescherichiacolicelldivision
AT typasathanasios coordinationofpeptidoglycansynthesisandoutermembraneconstrictionduringescherichiacolicelldivision
AT grosscarola coordinationofpeptidoglycansynthesisandoutermembraneconstrictionduringescherichiacolicelldivision
AT vollmerwaldemar coordinationofpeptidoglycansynthesisandoutermembraneconstrictionduringescherichiacolicelldivision